Raising Awareness of the Threat of Fusarium Wilt Tropical Race 4 in Latin America and the Caribbean

Raising Awareness of the Threat of Fusarium Wilt Tropical Race 4 in Latin America and the Caribbean L.E. Pocasangre 1, R.C. Ploetz 2, A.B. Molina 3 and L. Perez Vicente 4 1 Bioversity International, Commodities for Livelihoods Programme for Latin America and the Caribbean, Campus CATIE, Turrialba, Costa Rica 2 Tropical Research and Education Centere, Homestead, University of Florida, USA 3 Bioversity International, Commodities for Livelihoods Programme for Asia Pacific, Campus IRRI, Los Banos, Philippines 4 INISAV, Plant Protection and Quarantine of Cuba, Ciudad de La Habana, CP 11600, Cuba Keywords: action plan, banana and plantain, INISAV, MUSALAC, OIRSA, Panama disease, quarantine, risk analysis, stakeholders Abstract Banana and plantain are among the most important commodities, both as staple food and as export crop, for many countries in Latin America and the Caribbean. Fusarium oxysporum f. sp. cubense (Foc) tropical race 4 (TR4), which is attacking banana in Asia, represents a threat to the export banana industry which in Latin America is based almost 100% on the Cavendish subgroup that is susceptible to Foc TR4. Production for national markets, based on apple banana, plantain and Gros Michel, is also under threat. Bioversity International has formed a strategic alliance with the Research and Development Network for Plantain and Banana for Latin America and the Caribbean (MUSALAC), the Regional Organization for Agriculture and Livestock Sanitation (OIRSA), the University of Florida and the Cuban Instituto Nacional de Investigacion de Sanidad Vegetal (INISAV) to launch an awareness campaign in order to prevent entrance of Foc TR4 into the Americas. The threat of Foc TR4 was first raised in the VII Steering Committee meeting of MUSALAC held in Panama in October 2007. The 12 country representatives prepared a resolution emphasising the importance of quarantine measures. The resolution of this workshop has been distributed to all 13 MUSALAC member countries. In addition, OIRSA sent an official communication to the agriculture ministries of nine countries in Central America in order to strengthen the quarantine measures of plant protection departments to prevent entrance of this pathogen. In addition to the resolution and actions by OIRSA, Bioversity International and OIRSA are co-organising a training workshop and expert consultation with country quarantine officers and international Fusarium specialists. The workshop will provide technical training to country representatives and input to prepare quarantine guidelines oriented to all stakeholders of the banana production chain and other related sectors such as ornamental plants. IMPORTANCE OF THE BANANA INDUSTRY FOR LATIN AMERICA AND THE CARIBBEAN Banana is one of the most important commodities, not only for foreign exchange generation for producing countries, but also as food security for rural and urban populations of several countries in the region. In addition, with its year-round production, banana is one of the few commodities that provide a permanent source of employment for rural populations. For example, Ecuador has more than 225,000 ha cultivated with banana, creating more than 500,000 jobs that depend directly or indirectly on this industry and generating 1350 million dollars per year (V.H. Quimí, pers. commun.). In the case of Costa Rica, the second largest exporter in the region, more than 43,000 ha of banana cultivation create more than 100,000 jobs generating 659 million dollars per year (Pocasangre and Perez Vicente, 2009; Sandoval and Segura, 2009). Fusarium wilt of banana caused by Fusarium oxysporum f. sp. cubense (Foc) has Proc. Int l ISHS-ProMusa Symp. on Global Perspectives on Asian Challenges Eds.: I. Van den Bergh et al. Acta Hort. 897, ISHS 2011 331

been considered the most destructive disease in banana (Stover, 1962; Stover and Buddenhagen, 1986; Ploetz, 1994, 1998, 2006; Turstone, 1997). The destruction of the cultivar Gros Michael (AAA) by Fusarium wilt is a classic example of the aggressiveness of the pathogen and the dangers associated with monoculture of a crop (Stover, 1962). After replacing the susceptible Gros Michel with cultivars from the Cavendish (AAA) subgroup that are resistant to Foc race 1, the Fusarium wilt nightmare was soon forgotten. Currently, all commercial banana plantations in the region are cultivated with Cavendish, and even organic production is based 100% on Cavendish cultivars. According to Lescot (2008), Cavendish production reaches 17.73 million tonnes and represents 46% of all bananas cultivated in Latin America and the Caribbean (LAC). But since the Cavendish cultivars are not resistant to Foc tropical race 4 (TR4), this genetically homogenous monocrops production system creates the perfect conditions for a Foc TR4 epidemic in the region. In addition, according to a risk analysis conducted by Ploetz (2009), the probability of the entrance of TR4 via accidental route or bioterrorism is higher than 80%. Molina et al. (2009) report that the disease is rapidly spreading in Asia and the Pacific, and represents a menace to the Americas. Therefore, we need to take all the necessary actions in order to prevent entrance of this pathogen to the region. CURRENT STATUS OF FUSARIUM WILT IN LATIN AMERICA AND THE CARRIBEAN Fusarium wilt is still causing damage on susceptible cultivars which are cultivated mainly for local consumption by small farmers in Latin America and the Caribbean. The most important susceptible cultivars attacked by Foc are Gros Michel, apple banana (AAB), Prata (AAB) and cooking bananas like Bluggoe (ABB). In all places where susceptible cultivars are planted, Fusarium wilt is causing serious damage. In the present paper, we will call it a pathosystem according to the susceptible cultivar affected. Pathosystem I: Fusarium Wilt Race 1 on Gros Michel Traditionally, coffee is one of the most important commodities in LAC, and normally it is cultivated with Gros Michel as a shade crop. However, in many cases, banana becomes the major crop in the system as it produces during the whole year while coffee only has two harvests a year. A survey conducted by Silagyi and Pocasangre (2003) indicates that 91% farms cultivated with Gros Michel and coffee intercropping in the region of Turrialba are affected by Fusarium wilt. The percentage of diseased plants reached up to 15.81% (Table 1). The same authors conducted a survey on Gros Michel in intercropping with cacao in the region of Talamanca, and the results indicated that 40% of the surveyed farms were affected by Foc race 1, and the disease incidence was just 1.4% (Table 2). It is important to point out that the lower disease incidence found in the Talamanca region can be associated with the fact that Gros Michel is cultivated in low densities and intercropped with timber trees for which the soils organic matter is more diverse in natural micro-organisms that can have a natural biocontrol activity to Foc. Pathosystem II: Fusarium Wilt Race 1 on Apple Banana Like Gros Michel, apple banana is considered one of the best dessert bananas and is in high demand by consumers, who agree to pay a higher price in comparison to Cavendish. In Trujillo in Venezuela, 1500 ha devoted to apple banana for export were destroyed by Foc race 1 (Rodriguez, 2009). Currently, farmers are still cultivating apple banana in annual cropping systems, rotating it with Cavendish in order to reduce the Foc inoculum; in this way, they can plant apple banana every 2 years in the same place. In Mexico, in the state of Nayarit, more than 2600 ha of apple banana have been destroyed by Foc race 1; however, farmers are still cultivating it for the local market (Orozco et al., 2009). Currently, there are approximately 600 ha of apple banana in Mexico, but there is no production of Gros Michel, whose local name is Roatan. Destruction of apple banana in the tropical areas of Cochabamba, Bolivia, and in the Amazonia of Brazil has been reported by Bohorquez (pers. commun., 2003) and Gasparoto (pers. commun., 2007), 332

respectively. Pathosystem III: Fusarium Wilt Race 1 on Prata Brazil is the only country in South America where the population has developed a preference for Prata banana, and the consumers are paying a higher price for the fruit than for Cavendish. Fusarium wilt is affecting Prata cultivars, and the worst case is seen in the Manaus region located in the Amazonia where susceptible cultivars have been replaced by resistant EMBRAPA and FHIA hybrids (L.E. Pocasangre, unpublished data). In the Atlantic coast of Santa Catarina in Brazil, there are more than 10,000 ha planted with Prata, specially the Enxerto cultivar. However, from time to time, it is more difficult to manage Fusarium wilt, and therefore, farmers are replacing Prata with Cavendish cultivars, specially Grande Naine and Nanicon (Hinz et al., 2009). Currently, there are some problems with Fusarium, caused by Foc race 1, on Cavendish. This particular Cavendish susceptibility has been associated to low temperatures which predispose the plant to Foc attack. Pathosystem IV: Fusarium Wilt Race 2 on Bluggoe Bluggoe cooking banana has been extensively reported as susceptible to Foc race 2 (Stover, 1962, 1972; Stover and Buddenhagen, 1986). Currently, this cooking banana is extensively cultivated in some countries of the region, such as Nicaragua, Venezuela, Peru and Ecuador. It is playing a key role in food security in rural areas and it is an important source of carbohydrates for the population in the region. Unfortunately, there is no information about incidence and severity of Fusarium wilt on Bluggoe. However, the disease is present in all countries where Bluggoe is cultivated. In the case of Venezuela, race 2 has been reported in five states, and a total of 20 isolates have been recovered and confirmed as Foc race 2. In the case of Nicaragua, in the region of Tola, Rivas, Fusarium has been identified and it is the major disease affecting Bluggoe, followed by Moko bacterial wilt, caused by Ralstonia solanacearum (L.E. Pocasangre, unpublished data). Pathosystem V: Fusarium Wilt in Backyards Traditionally, farmers all over the world cultivate the banana cultivars of their choice in their backyards. Unfortunately, most of these cultivars are susceptible to Foc race 1 and race 2. Therefore, it is very common to find Fusarium wilt cases in all countries of the region. In addition, apparently healthy banana planting material taken from backyards is an important dissemination source of Foc race 1 and race 2. Furthermore, it is very common to find combined infections of Fusarium wilt and Moko bacterial wilt, especially in Bluggoe and apple banana which are highly susceptible to both pathogens. It is important to point out that no confirmed cases of Fusarium wilt have been reported in areas where plantain is cultivated, like in the Ulua Valley in Honduras, Tiquizate in Guatemala, Puerto Armuelles and Baru in Panama, which are highly infested by Foc race 1; this is due to the plantain s resistance to Foc race 1 and race 2. In consequence, it is important to keep Foc TR4 away from the region in order to protect the plantain industry. It is also important to point out that if any cases of Fusarium wilt appear on plantain in Central America under tropical conditions, we need to process the samples for specific Foc TR4 diagnostic. AWARENESS CAMPAIGN ON FUSARIUM OXYSPORUM F. SP. CUBENSE TROPICAL RACE 4 FOR LATIN AMERICA AND THE CARIBBEAN Since 7 years, Bioversity International has been raising awareness in the banana and plantain industry of the region about the real threat of Foc TR4. As a result of several discussions with pathologists in the region and the resolution on Foc TR4 stated by the MUSALAC Steering Committee in October 2007, we launched an awareness campaign through which it has been possible to discuss the menace of this pathogen in several congresses of the region: (1) the V Forum of Banana and Fresh Fruit in Guayaquil, Ecuador, April 2008; (2) the International Soil and Root Health Congress in Maracay, 333

Venezuela, July 2008; (3) the Special presentation to the Executive Director of the Regional Organization for Agriculture and Livestock Sanitation ( OIRSA), October 2008; (4) the XVIII International Meeting of ACORBAT, Guayaquil, Ecuador, 2008; (5) the II International Banana Congress in Argentina, Oran Salta, Argentina, April 2009; (6) the Special presentation to the OIRSA Steering Committee, San Salvador, El Salvador, May 2009; (7) the I International Plantain and Banana Congress in Venezuela, Santa Barbara, Zulia, Venezuela, June 2009; and (8) the Stakeholders Meeting on Foc Tropical Race 4 and Banana bunchy top virus (BBTV) in alliance with OIRSA in San Salvador, July 2009. Action Plan to Prevent Entrance of Foc TR4 and BBTV The stakeholders meeting on Foc TR4 and BBTV has special historical importance, as it was attended by representatives from 14 countries of the region, including plant protection departments, grower associations from nine countries, multinational companies such Chiquita, Dole, Del Monte and Bayer as well as several international research institutes and universities. The most important product of the stakeholders meeting was an action plan to prevent entrance of both pathogens. The most important points considered in the action plan are: 1. To evaluate current quarantine measures in several countries and to strengthen inspection measures in ports of entry of the western hemisphere: - To assess national and regional phytosanitary regulations to reduce entrance risks of Foc TR4 and BBTV, as well as to strengthen border interception capacities, early detection, contention and possible eradication of eventual Foc TR4 and BBTV outbreaks; - To include Foc TR4 and BBTV on the A1 list of countries quarantine diseases; - After conducting a risk analysis, to allow banana and plantain propagation materials coming from countries where these diseases are already present to enter only through intermediate quarantine stations; Introduction of in vitro plants must be accompanied by a certificate of indexation for diseases; - To determine and strengthen entrance points with higher risks of becoming paths for introducing plants or materials which are potential Foc TR4 and BBTV carriers; - To develop a legislation and phytosanitary regulation that will guarantee patrolling and also the obligation to make a declaration of plants or parts of plants and risky material to be introduced from any affected country as well as local disease outbreaks and the establishment of contention, eradiation and/or management measures; - To standardise the regulation s content and format, the training documents and materials and the diseases alerts in OIRSA member countries and in other LAC countries; - To start an emergency fund with the input of the ministries of agriculture and partners of the banana production and commercialisation process to detect, content and eradiate eventual Foc TR4 outbreaks. 2. To develop an entrance risk analysis for Foc TR4 and BBTV in the region and in the countries: - To complete a risk analysis of Foc TR4 and BBTV entrance; - To determine the highest risk entrance points in countries to provide training in order to strengthen the capacity to intercept banana and other plants considered as potential Foc TR4 and BBTV hosts. 3. To increase governments and public awareness regarding the impact that Foc TR4 and BBTV entrance can have in LAC: - To announce, using numbers, the economic and social impact that Foc TR4 and BBTV have caused to the countries where they are already present; - To develop awareness campaigns among producers, technicians and the general public about the harmfulness and the risks of Foc and BBTV entrance, and its relationship to moving materials from infected countries. 334

4. To train technical personnel and producers on the entrance paths of both diseases to LAC: - To train quarantine and customs officers in regards to entrance risks of both diseases in host plant materials and also about regional regulations regarding them; - To train extensionists, production technicians and state services of plant protection staff about both diseases with emphasis on learning how to recognise them and the conditions for their establishment and development; - To distribute posters, brochures and information videos about the diseases on border points, enterprises and producer organisations; - To prepare technical material and development of Foc and BBTV workshops about detection, contention and eradiation procedures of plants diagnosed as positive; - To distribute scientific articles and proceedings of international events and workshops. 5. To develop as soon as possible sensitive and reliable methodologies for early Foc TR4 detection and to disseminate BBTV diagnostic protocols: - To prioritise through international scientific institutions the acquisition, validation and availability of a specific and efficient diagnostic system for Foc TR4 detection; - To define and develop capacities in laboratories approved by the Plant Protection Service to diagnose Foc TR4 and BBTV; - To establish the regulations, protocols, procedures, responsibilities and faculties to sample, to transport samples and to conduct laboratory diagnostics; - To train personnel in production places in detecting plants with disease symptoms. 6. To develop databases of Foc populations in LAC: - To look for financing to determine Foc populations present in the countries; - To coordinate this with international institutions and other groups working in this area. CONCLUSIONS Race 1 of Foc is widespread in LAC and it is still attacking susceptible Gros Michel, apple banana and Prata cultivars in all countries. Race 2 of Foc is also spread in the region and it is attacking cooking bananas in small plantations, mainly in backyards of rural areas in LAC. Tropical race 4 of Foc is not present in LAC, and therefore, it is urgent that plant protection departments in the whole region start implementing the action plan that resulted from the stakeholders meeting on Foc TR4 in order to prevent entrance of this pathogen to the region. BBTV is not present in the region and to avoid entrance of this pathogen, it is necessary to follow the same steps as for Foc TR4. However, special attention must be given to in vitro plants commercialisation, as the virus can be transmitted during the micropropagation process. Literature Cited Hinz, R., Silva, C.M., Pereira, A. and Tcancenco, F.A. 2009. Análisis de la diversidad genética de Fusarium oxysporum f. sp. cubense en el estado de Santa Catarina, Brasil. p.25-26. In: Proceedings of the Stakeholders Meeting on Tropical Race 4 of Fusarium and BBTV, San Salvador, El Salvador, July 2009. Lescot, T. 2008. The genetic diversity of banana in figures. FruiTrop, CIRAD, France. N155:29-33. Molina, A.B., Fabregar, E., Sinohin, V.G., Yi, G. and Viljoen, A. 2009. Recent occurrence of Fusarium oxysporum f. sp. cubense Tropical Race 4 in Asia. Acta Hort. 828:109-115. Orozco, M., Garcia, K. and Vázquez-Jiménez, J.L. 2009. Estado actual del Mal de Panamá en Musaceas en México. p.30. In: Proceedings of the Stakeholders Meeting on Tropical Race 4 of Fusarium and BBTV, San Salvador, El Salvador, July 2009. Ploetz, R.C. 1994. Panama disease: return of the first banana menace. International Journal of Pest Management 40(4):326-336. 335

Ploetz, R.C. 1998. Banana disease in the subtropic a review of the importance distribution and management. Acta Hort. 490:263-276. Ploetz, R.C. 2006. Fusarium wilt of banana is caused by several pathogens referred to as Fusarium oxysporum f. sp. cubense. Phytopathology 96:653-656. Ploetz, R.C. 2009. Assessing threats posed by destructive banana pathogens. Acta Hort. 828:245-251. Pocasangre, L.E. and Perez Vicente, L. 2009. Impacto potencial de la entrada de Raza Tropical 4 del Mal de Panamá Fusarium oxysporum f. sp. cubense en la industria bananera y platanera de América Latina y el Caribe. p.24. In: Proceedings of the Stakeholders Meeting on Tropical Race 4 of Fusarium and BBTV, San Salvador, El Salvador, July 2009. Rodríguez, D. 2009. Estado actual del Mal de Panamá en banana manzano (AAB) y Bluggoe (ABB) en Venezuela. p.29. In: Proceedings of the Stakeholders Meeting on Tropical Race 4 of Fusarium and BBTV, San Salvador, El Salvador, July 2009. Sandoval, J. and Segura, R. 2009. Investigación desarrollo e innovación en la producción de banano (Musa AAA) en Costa Rica. p.23. In: Proceedings of the Stakeholders Meeting on Tropical Race 4 of Fusarium and BBTV, San Salvador, El Salvador, July 2009. Silagyi, A.J. and Pocasangre, L.E. 2003. Current status of Fusarium wilt on Gros Michel in smallholdings in Costa Rica. p.12. In: Proceedings of 2nd International Symposium on Fusarium Wilt on Banana, Salvador de Bahia, Brazil, September 2003. Stover, R.H. 1962. Fusarium Wilt (Panama Disease) of Banana and other Musa Species. Phytopathology paper 4. Commonwealth Mycological Institute, Kew Surrey, England. Stover, R.H. 1972. Banana, Plantain and Abaca Diseases. Commonwealth Mycological Institute, Kew Surrey, England. Stover, R.H. and Buddenhagen, I. 1986. Disease management strategies and survival of the banana industry. Annual Review of Phytopathology 24:83-91. Turstone, H.D. 1997. Tropical Plant Diseases. 2nd Edition. American Phytopathology Society, St. Paul, MN. 336

Tables Table 1. Incidence of Fusarium wilt, caused by Fusarium oxysporum f. sp. cubense (Foc), on Gros Michel in intercropping with coffee in the region of Turrialba, Costa Rica. Farmer Community Foc presence Foc incidence (%) Allan Esquivel Azul + 18 Efrain Araya Pejibaye + 5 Gerardo Leiva Javillo + 43 Alvaro Fuentes Tres X + 39 Cenon Camacho Platanillo + 3 Juan Fallas Platanillo - 0 Edgar Rodriguez Chitaria + 4 Jose Calvo Sitio Mata + 17 Carlos Contreras Sitio Mata + 9 German Mora San Antonio + 21 Rigoberto Soto Chitaria + 15 Average 91% 16 Table 2. Incidence of Fusarium wilt, caused by Fusarium oxysporum f. sp. cubense (Foc), on Gros Michel in intercropping with cacao in the region of Talamanca, Costa Rica. Farmer Community Foc presence Foc incidence (%) Wilfred Brown Watsi - 0 Elsa Lopez Watsi - 0 Agristina Morales Watsi - 0 Ruperto Romero Amubri + 7.1 Mauricion Blanco Amubri - 0 Roger Paez Amubri - 0 Bertilio Jimenez Amubri + 1.4 Encarnacion Pereira Carbon 1 + 3.7 Luis Rodriguez Bribi - 0 Edwin Patterson Cocles + 1.8 Average 40% 1.4 337